Anxious about rejection, avoidant of neglect: Infant marmosets tune their attachment based on individual caregiver’s parenting style

Children’s secure attachment with their primary caregivers is crucial for physical, cognitive, and emotional maturation. Yet, the causal links between specific parenting behaviors and infant attachment patterns are not fully understood. Here we report infant attachment in New World monkeys common marmosets, characterized by shared infant care among parents and older siblings and complex vocal communications. By integrating natural variations in parenting styles and subsecond-scale microanalyses of dyadic vocal and physical interactions, we demonstrate that marmoset infants signal their needs through context-dependent call use and selective approaches toward familiar caregivers. The infant attachment behaviors are tuned to each caregiver’s parenting style; infants use negative calls when carried by rejecting caregivers and selectively avoid neglectful and rejecting caregivers. Family-deprived infants fail to develop such adaptive uses of attachment behaviors. With these similarities with humans, marmosets offer a promising model for investigating the biological mechanisms of attachment security.

Supplementary Figure 2 Infant behaviors in the retrieval assay using family-reared infants.
a Segmented regression analysis of the rejection-call interval.The inflection point could not be determined; thus, we also used the 9.4-second offset obtained from movement analysis (Fig. 2d) for call analysis.A total of 77.18% (3981 out of 5158) of the infant calls during carrying occurred during and within 9.4 sec after the preceding rejection.d Violin plot of the call frequency of male and female infants during Alone_BeforeRET.The numbers within parentheses are the numbers of the trials.As the only sex difference identified in infant attachment behaviors (Fig. 1c), female infants called more than male infants when the infants were alone before the first retrieval (GLMM).This effect was not attributed to the sexual difference in body size growth, as there was no correlation between the isolation calls and body weight (Supplementary Figure 2e).More avoidant behaviors were observed in the dyad with longer retrieval latency (t = 2.76, p = 0.0078), although the infant calls during carrying were not different from those in the other dyad.
In the dyad with a higher %Rejection, the infant calls during carrying and the avoidant behaviors were more frequent (call-during-carrying: t = 5.13, p < 0.001, avoidant behavior: t = 4.323, p < 0.001).In the dyad with a higher %Carrying than the average, the infant calls during carrying and the avoidant behaviors were less frequent (call-during-carrying: t = -4.25,p < 0.001, avoidant behavior: t = -7.367,p < 0.001).Each dot shows the value of each session, and the same color

b
Fig. 2j.Only the data with detailed vocal analysis were included.The numbers within the parentheses are the numbers of the sessions.Each dot shows the total call frequency in each session.Data was collected from 166 sessions of 35 dyads.
(199 sessions of 55 dyads) e Scatter plot of body weight and infants' call frequency during Alone_BeforeRET.The call frequency was not affected by body weight (GLMM).Female: orange, male: green.(155 sessions of 50 dyads) Supplementary Figure 3 Vocal behaviors in isolation.a-f The mean ± s.e.call frequencies in the isolated recordings (Art: n = 1 male; Cont: n = 9 (4 males, 5 females).Total calls (a) as well as phee (b), cry (c), tsik (d), trill (e), and twitter calls (f).Each dot shows the value in each session.g The mean ± s.e. total calls and composition of call types of Cont (left) and Art infants (right).Error bars represent the standard error of the total calls.Each dot shows the number of total calls in each session.The left is the same as in Fig. 2l, shown for comparison.Supplementary Figure 4 Relationship between caregiver and infant behaviors in the retrieval assay using family-reared infants.a Representative raster plots of the retrieval assay using a pair of littermates and their parent.See text for explanation.Black triangles: dismounting without preceding rejection within 9.4 sec.Red triangles: refusal to cling when contacted.Left two plots were also shown in Fig. 3a-b.b-c Variation in caregiving (b) and attachment behavior (c) during postnatal weeks 0-3 (54 dyads, excluding one dyad in which the caregiver never retrieved the infant).Each point represents the value averaged for each caregiver-infant dyad, with the color of each caregiver (warm colors: females, cold colors: males).The marker shapes indicate each breeding pair.Labels near markers are the first two letters of the caregiver's and infant's names.For example, dark blue for Tochan, pink triangles for Kachan.The vertical and horizontal lines show the mean + 1 s.d.d Frequency of infant calls during carrying and the number of avoidant behaviors averaged for each dyad.Upper: both %Rejection and the log of RET_Latency were less than the mean + 1 s.d.(n = 36), lower: the other dyads (n = 18).Two-dimensional probability density was overlaid as a contour with 10 bins.Vertical and horizontal lines indicate the mean + 1 s.d. for each axis.e Scatter plots and regression lines of infant calls during carrying (top) and avoidant behavior (bottom) and caregiving parameters (left: RET_Latency, center: %Rejection, right: %Carrying).
indicates data from the same caregiver.(199 sessions of 55 dyads.For %Rejection and call during carrying, 185 sessions of 54 dyads, as sessions without first retrieval were excluded.)f Violin plots of the infant calls during holding (top) and transport (bottom) in the groups of dyads divided by high/low parental behaviors(RET_Latency, %Rejection, %Carrying).Each dot shows the value of each session, and the color indicates the individual caregiver.The filled circles and error bars show the mean ± s.e.The numbers within parentheses are the numbers of the sessions.(185sessions of 54 dyads, as sessions without first retrieval were excluded.)GLMMs were used for statistical analyses.**: p < 0.01, ***: p < 0.001Supplementary Figure 5 Family reunion observation with artificially reared infants.A Schematic of the behavioral tests of artificially reared (Art) and control (Cont) infants.B Representative raster plot of family reunion observation.One Art and two Cont littermate infants at PND 31 were returned to their family cages one by one.The Art infant Senazo (the bottom row) was first retrieved by the father but soon dismounted because of the father's rejection (dark blue bins).The experimenter assisted Senazo in clinging to the mother, which was tolerant and was carrying two Cont infants (Yoshie and Shirizo, the top and middle row).The mother carried three infants (10th to 20th pink bins) and then rejected them (the 21st dark purple bin).Senazo dismounted, while two Cont littermates kept clinging even though the mother kept rejecting them for 6 consecutive bins.In the meantime, Senazo came into contact with the brother (24th-26th light green bins) but did not cling to the brother (retrieval refused by the infant, orange mark above the bin).Senazo called in two long bouts from the 29th and 46th bins (yellow marks), and came into contact with the brother and the father sequentially but refused to cling.The two Cont infants did not call while being alone after dismounted from the father at the 34th bin, which showed ageappropriate maturity.In contrast, Senazo showed excessive distress calls (which should attract caregivers) but avoided simultaneously, the behavior reminiscent of "disorganized" attachment in humans.In addition, compared to Cont littermates, Senazo tended to give up clinging and dismount easily by brief rejection.Bin: 10-sec.c-eThe duration of a carrying bout (c), the latency of the first rejection (d), and the number of caregivers' rejection bins (e) in a carrying bout were calculated.A carrying bout is a period from the bin when an infant starts to cling onto a caregiver to the bin when the infant dismounts from the caregiver or moves to another caregiver.The shape and color of the markers represent each infant.cTheduration of a carrying bout (Cont: 363 bouts, Art: 299 bouts) was shorter among the older infants (t = -5.63,p < 0.001).dThe latency of the first rejection in a carrying bout (Cont: 323 bouts, Art: 244 bouts) was shorter among the older infants (t = -5.10,p < 0.001).eIn the number of caregiver rejection bins (Cont: 363 bouts, Art: 299 bouts), the interaction effect of Art and PND was significant (z = -7.65,p < 0.001), indicating that the coefficient of PND among the artificially reared infants was smaller than that among the family-reared infants.Statistical analyses were performed by the generalized linear mixed model (GLMM).*: p < 0.05, **: p < 0.01, ***: p < 0.001